Macquarie University scientists have discovered that when it comes to calculated duplicity, it’s hard to beat a mourning cuttlefish (Sepia plangon). The male squids have been found not only to simultaneously “lie” to competitors whilst courting female squid, but to also make value judgments as to when it is safest to do so.

In naturally occurring populations of mourning squid, males outnumber females, prompting males to compete for access to receptive females. Male and female mourning cuttlefish can be distinguished from one another by their arms. Males have significantly longer arms than females do, which are modified to enable the transfer of the spermatophore, a sort of sperm parcel the males pass to the females during mating.

Like other cephalopods, mourning cuttlefish are able to rapidly change their skin’s colour and texture. They use this talent both to signal to other squid, and to conceal themselves from potential predators and prey. Male cuttlefish tend to adopt flashy patterns of pulsating stripes around other species (interspecifically), whilst females are more likely to adopt a more mottled, camouflaged patterning during such interactions, to blend into the landscape. Although squids may “lie” to other species, impersonating rocks to avoid detection, they don’t usually lie when signalling to other squids (intraspecifically) – this behaviour is socially punished, and therefore, not often practiced.

Animal communications theory suggests that honesty is the most evolutionarily stable strategy within a population. If most of the animals within your group signalled dishonestly, these “lies” would lead to general mistrust. All statements would be open to challenge, perhaps in the form of physical combat, which would not benefit persistent liars, or the population, in the longer term. This makes honesty the best policy at a group level. However, if the potential benefits of false signalling for an individual are high enough, and the potential costs are sufficiently low, cheating can be a risk worth taking.

Mixed messages
The scientists found that male squids with an interest in a female squid would covertly signal his masculine interest with one half of his body, while showing a softer, faux-feminine side to competing males in 39% of such interactions. While previous studies have observed male squids masquerading as females for mating advantage, and others have observed bilateral asymmetry in patterning as a predator evasion device, this is the first study which has observed these behaviours co-occurring.

Through careful alignment and by changing the patterning on either side of their bodies with split-second precision, the male cuttlefish are effectively able to maintain two, more-or-less private conversations. While one half of their body is saying something like “oh, don’t mind me, I’m just a not-especially-interesting-camoflagued-girly-cuttlefish,” to a passing male on one side, their other flank, visible to the female squid, is like “Hey there, sexy laydee! I gotta whole lotta spermatophore love fo’ you!” If these signals of love are favourably received by the female in question, the smooth-talking male and his new love get down to swapping more than phone numbers, uninterrupted by the oblivious nearby male.

Discretion – the greater part of valour
Obviously, male cuttlefish can’t just go shouting their love from the reef-tops. Communications theory states that for each message, or signal, a sender produces, there is an intended receiver. In this case, the signaller is the randy male squid; the receiver, the favoured female. However, visual signals, like skin coloration and texture in squids, are often not especially discreet, and can be picked up on by “eavesdroppers” – unintended recipients of the signal. As such, as a male squid, it makes sense to be selective about when you signal an interest in a female, lest other males notice and interfere with your courtship efforts.

The scientists hypothesised that male squids would only “cheat” by sending out these deceptive signals to nearby males when they were unlikely to be discovered fibbing by their rivals. Their hypothesis was supported by the study results – squids don’t just cross-dress willy-nilly.

Male squids only try it on when conditions are highly favourable – that is, when a female is on one side, and only one other male is on the other. Should there be more than one male, it could be difficult to effectively maintain the faux-female facade, and the lying male would be liable to be exposed and punished. If there is more than one female present, the males also don’t bother with this pretence, perhaps because of the difficulty in signalling interest to two females whilst simultaneously signalling faux-femininity to a nearby male.

According to the study authors “these observation suggest that cuttlefish cognition is sophisticated……Tactical infraspecific deception in animals is commonly associated with higher vertebrates because of its link with sophisticated cognitive function.” A comparable example in the primate world is seen where female and subdominant male gorillas sneak off to mate surreptitiously while the dominant silverback’s not looking.

Due to their comparable brain size and complexity, cephalopods, while bright for molluscs, were not considered to harbour intellects comparable to those of advanced primates, however their tactical intraspecific fibbing may be “indicative of highly complex behaviour that includes mimicry, tool use and tactical deception.” As social animals, the cuttlefish appear to have picked up some of the smarts we’ve previously assigned only to primates.

Squid. They’re two-faced, multi-tasking, and smarter than we thought; don’t turn your back on the ocean.